Original article
Ultrasonographic tissue characterisation of human
1Department of Orthopaedics,
Erasmus university Medical
Centre, Rotterdam, The
Netherlands
2Department of Equine
Sciences, Utrecht university,
Utrecht, The Netherlands
3 The Hague Medical Centre
Antoniushove, Leidschendam,
The Netherlands
4Leiden Institute of Advanced
Computer Science, Leiden
University, Leiden, The
Netherlands
Correspondence to
Dr H T M van Schie,
Department of Orthopaedics,
Erasmus University Medical
Centre, PO Box 2040, 3000 CA
Rotterdam,
Dr Molenwaterplein 50,
Room Ee1614, Rotterdam
3015, The Netherlands;
j.vanschie@erasmusmc.nl
Accepted 22 June 2009
Published Online First
6 August 2009
Br J Sports Med 2010;44:1153–1159. doi:10.1136/bjsm.2009.061010
Achilles tendons: quantification of tendon structure
through a novel non-invasive approach
H T M van Schie,1,2 R J de Vos,1,3 S de Jonge,3 E M Bakker,4 M P Heijboer1
J A N Verhaar,1 J L Tol,3 H Weinans1
ABSTRACT
Objective To assess whether three-dimensional
imaging of the Achilles tendon by ultrasonographic
tissue characterisation (UTC) can differentiate between
symptomatic and asymptomatic tendons.
Design Case-control study.
Setting Sports Medical Department of the Hague
Medical Centre.
Patients Twenty-six tendons from patients with
chronic midportion Achilles tendinopathy were
included. The “matched” control group consisted of 26
asymptomatic tendons.
Interventions Symptomatic and asymptomatic
tendons were scanned using the UTC procedure.
One researcher performed the ultrasonographic data
collection. These blinded data were randomised,
and outcome measures were determined by two
independent observers.
Main outcome measurements The raw
ultrasonographic images were analysed with a custom-
designed algorithm that quantifies the three-dimensional
stability of echo patterns, qua intensity and distribution
over contiguous transverse images. This three-
dimensional stability was related to tendon structure in
previous studies. UTC categorises four different echo-
types that represent (I) highly stable; (II) medium stable;
(III) highly variable and (IV) constantly low intensity and
variable distribution. The percentages of echo-types
were calculated, and the maximum tendon thickness
was measured. Finally, the inter-observer reliability of
UTC was determined.
Results Symptomatic tendons showed less pixels in
echo-types I and II than asymptomatic tendons (51.5%
vs 76.6%, p<0.001), thus less three-dimensional
stability of the echo pattern. The mean maximum tendon
thickness was 9.2 mm in the symptomatic group and
6.8 mm in the asymptomatic group (p<0.001). The
Intraclass Correlation Coefficient (ICC) for the inter-
observer reliability of determining the echo-types I+II
was 0.95. The ICC for tendon thickness was 0.84.
Conclusion UTC can quantitatively evaluate tendon
structure and thereby discriminate symptomatic and
asymptomatic tendons. As such, UTC might be useful to
monitor treatment protocols.
INTRODUCTION
The Achilles tendon is a hierarchically arranged
structure with a collagenous matrix in the direc-
tion of tensile forces transferred through the
tendon.1
Midportion Achilles tendinopathy is the clini-
cal designation used for a painful swollen Achilles
tendon at 2–7 cm proximal to the tendon insertion
with an impaired function. 2 3 In these tendons, a
remarkable matrix disintegration can be found as
a consequence of degeneration. Biochemically, a
young matrix with high collagen turnover and
a tendency to fibrotic repair is observed.4 These
phenomena are elements of the histopathological
label “tendinosis”. 5
On ultrasonography, the echogenicity of ten-
dons is based on the density and arrangement of
the collagenous matrix. Normal tendons are char-
acterised by a regular echo pattern, qua inten-
sity and arrangement in grey scale images.6 7 On
the contrary, disintegration of tendon bundles
leads to a remarkable loss of the echogenicity.
Consequently, hypoechoic lesions are frequently
described in cases of tendinosis.8
There are some sonographic studies that evalu-
ated the possible difference between symptomatic
and asymptomatic tendons. One study reported
only hypoechoic areas in 68% of the symptom-
atic Achilles tendons,9 but another group found
hypoechoic areas also in 11% of asymptomatic
tendons.10 Some studies focused on the prognos-
tic value of hypoechoic lesions. No difference was
found in overall outcome after conservative treat-
ment between tendons with normal ultrasono-
graphic appearance and tendons with a hypoechoic
area.11 Khan et al12 reported that a reduced area of
hypoechogenicity on ultrasonography did not cor-
relate with an improved clinical outcome.
The main problem with ultrasonography is
that it is a real-time and operator-dependent tech-
nique; transducer handling and machine settings
can influence size and appearance of a hypoechoic
lesion. To our knowledge, the inter-observer reli-
ability of ultrasonographic assessment of tendon
structure is not known, and changes in time are
difficult to compare. Furthermore, the structure of
the (disintegrated) tendon is a three- dimensional
phenomenon that cannot be captured in fl at
two-dimensional transverse (nor longitudinal)
images.
There is growing interest in fi nding ways to
quantify tendon integrity.13 14 In veterinary medi-
cine, a method for computerised ultrasonographic
tissue characterisation (UTC) has been developed
for tendons in the horse.15 This work revealed that
each ultrasonographic image actually is a mixture
of “structure-related echoes” and “interference”.7
16 Structure-related echoes are directly generated
at tendon bundles and are stable over a large num-
ber of contiguous transverse cross sections. Echoes
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resulted from interference are the result of multiple echoes
generated by smaller entities, like fibrils, cells or fluid and are
variable over contiguous cross sections. Based on these equine
studies, four different echo-types were discriminated with use
of this three-dimensional stability criterion. With histology as
reference test, the echo-types reflected the underlying struc-
ture and pathology in the horse tendon tissue (fig. 1).15–19
The aim of this study is to evaluate UTC in the human set-
ting. Therefore, we determined its inter-observer reliability
and verified whether the technique could discriminate symp-
tomatic and asymptomatic tendons. The tendon thickness
was also determined.
MATERIALS AND METHODS
Patients
Patients were included in an outpatient sports medicine
department in a large district general hospital. Patients who
had participated in a previous study on the effect of an eccen-
tric exercise program at the sports medicine department were
included. 20 21 In this previous study, inclusion criteria were an
age between 18 and 70 years and presence of symptoms for
more than 2 months. All patients had a tendon, which was ten-
der on palpation and painful during or after activity. The ten-
don thickening was located approximately 2–7 cm proximal
to the distal insertion. The diagnosis was made based upon
clinical examination. Exclusion criteria were the presence of
an insertional disorder and complete tendon rupture. Most of
the patients had already received several types of conservative
treatment, but none had undergone surgery for their Achilles
tendon injury.
All patients with persistent pain on palpation or during
sports and <100 points on the Victorian Institute of Sport
Assessment-Achilles ( VISA-A) questionnaire, 22 which is a val-
idated instrument to quantify the clinical severity of Achilles
tendinopathy, were selected in the symptomatic group. The
activity of the lower extremity was evaluated with use of the
Ankle Activity Score (AAS), 23 which quantifies the ankle-
related activity level.
Ultrasonographic images of “matched” asymptomatic ten-
dons were collected from patients who visited the sports
medicine department for other injuries. When individuals
had not experienced pain in one of their Achilles tendons
in the past, they were asked to participate in the study for
evaluation of both their Achilles tendons. Inclusion was
based on matching the symptomatic group in age, gender
and activity level.
Ultrasonographic tissue characterisation
The UTC procedure and measurements were performed using
a standardised protocol (fig. 2). A 10-MHz linear-array trans-
ducer (Smartprobe 10L5; Terason 2000, Teratech, USA) was
moved manually along and perpendicular to the tendon’s long
axis over a distance of 9.6 cm. A custom-built tracking and
data-collection device facilitated the collection of “raw” digi-
tal transverse images at regular distances of 0.2 mm. These
images were stored on the hard disk of a computer and sub-
sequently composed to a three-dimensional data block. This
data block was used for the tomographical visualisation of the
Achilles tendon in three planes of view: transverse, sagittal
and coronal (fig. 3).

Figure 1 Ultrasonographic tissue characterisation (UTC) is based on a transducer in transverse position that is displaced stepwise in the
longitudinal direction. In this way, contiguous transverse images provide longitudinal information. The transducer emits ultrasound waves into
the tissue in the direction of the beam central axis. According to Harris et al,18 these waves form a three-dimensional sample volume that moves
through tissue. Every echo in the ultrasonographic image is the resultant of interactions/reflections that occur in this sample volume. Depending
of size of anatomical structure relative to the three-dimensional sample volume, echoes can be divided into “structure-related” and “interfering”.
Structure-related echoes (types I and II) are generated by only one large structure present in the sample volume, thus one interface and one
hit of ultrasound wave resulting in one really structure-related echo that is stable over a large number of contiguous transverse images while
the transducer moves along the tendon. In contrast, interfering echoes (types III and IV) represent more than just one smaller structure in the
same sample volume, thus multiple interfaces and multiple hits, and thus one echo is the resultant of multiple interfering ones. These echoes
are characterised by a remarkable lack of stability over contiguous transverse images. UTC algorithms were tested on isolated flexor tendons
collected from horses. By precise matching of UTC processed images with exactly corresponding tendon sections, echo-types were verified with
use of histology as reference test: (I) intact and aligned tendon bundles; (II) less integer and waving tendon bundles; (III) mainly fibrillar tissue and
(IV) a mainly amorphous matrix with loose fibrils, cells or fluid.7 15–17 19

1154 Br J Sports Med 2010;44:1153–1159. doi:10.1136/bjsm.2009.061010


The three-dimensional stability of the echo pattern, qua
intensity and distribution over contiguous transverse images
was analysed and quantified by means of custom-designed
algorithms for image analysis as developed on isolated
Figure 2 Standardised ultrasonographic tissue characterisation
procedure. The patients lay prone on the examination table with their
feet hanging over the edge of the examination table. The Achilles
tendons were manually positioned in a maximum angle of dorsiflexion
to ensure that the ultrasound probe was constantly perpendicular
to the tendon. A stand-off with scan gel was applied to the Achilles
tendon. The transducer was moved manually from proximal to distal
in a straight line along a frame over a distance of maximum 9.6 cm
with collection of images every 0.2 mm. These images were stored on
the hard disc of a computer and subsequently composed to a three-
dimensional data block.
Figure 3 Tomographic visualisation of a right Achilles tendon in three planes of view, in raw greyscale. (A) Transversal view. (B) Sagittal
view. (C) Coronal view. (D) Transversal view with the maximum antero-posterior thickness measured (white arrow), being the largest diameter
perpendicular to the latero-medial width of the tendon. At this position the outline of the Achilles tendon was drawn in the transverse image. This
cross-section was used for calculation of the percentages of echo-types within the tendon. S, skin; P, peritendinous space; AT, Achilles tendon;
CA, calcaneal bone.
Br J Sports Med 2010;44:1153–1159. doi:10.1136/bjsm.2009.061010
Original article
tendons collected from horses. 7 15–17 In these equine stud-
ies, four echo-types were assigned, based on the stability of
intensity and distribution in contiguous transverse images,
namely (I) highly stable; (II) medium stable; (III) highly vari-
able and (IV) constantly low intensity and variable distribu-
tion. Figure 1 summarises how underlying tissue structure
was related to the stability of the echo pattern. In the current
human study, we used the same UTC algorithms.
All datasets were blinded and randomised. Two research-
ers (HVS, RJV) performed the complete UTC processing and
analysis.
The thickest part of the tendon in the anterior–posterior
(AP) direction was identified, and the maximum thickness
was measured. After that, the border of the tendon was identi-
fied in the grey-scale image, and the percentages of the four
echo-types at the transverse cross-section at this site were cal-
culated (figs. 3 and 4). Also, at 2 mm proximal and 2 mm distal
from this position, the echo-types were calculated. The aver-
age of the echo-types in these three cross sections was used in
the overall assessment of the tendon.
Study design
The design was case-control study. The severity of the clinical
status of the symptomatic tendons was evaluated by a single
researcher, using the VISA-A questionnaire. 22
The inter-observer reliability was calculated with a one-
way random model. The intraclass correlation coefficient
(ICC) was used to evaluate the correlation between the obser-
vations of two researchers. To evaluate the ICC, one score per
observer per tendon was computed. The reliability is excellent
if the ICC is >0.75, fair to good if 0.4<ICC>0.75 and poor if ICC
is <0.4.15 To detect a difference in UTC parameters between
symptomatic and asymptomatic tendons, a Student t test was
1155
 Original article

used. Statistics were performed using SPSS version 15.0.0, and
significance was assumed for p values <0.05. The study pro-
tocol was approved by the Medical Ethics Committee of the
Hospital. Informed consent was obtained from all patients.
RESULTS
Patients
In both the symptomatic and asymptomatic groups, 26
Achilles tendons were included.
In the symptomatic group, there were 12 male and 14 female
tendons. In seven patients, symptoms were located in the left
Achilles tendon, three patients in the right tendon and eight
patients had bilateral complaints. The mean age was 44.9 years
(SD 6.2), mean duration of symptoms was 193.9 weeks (SD
277.5) and the mean body mass index was 24.8 kg/m² (SD 2.2).
The mean AAS was 4.8 (SD 2.0), and the mean VISA-A score
was 67.3 (SD 18.2).
In the asymptomatic group, there were 16 male and 10
female tendons. The mean age was 43.6 years (SD 12.6), and
the mean body mass index was 26.1 kg/m² (SD 4.3). The mean
AAS was 5.5 (SD 1.6).
There was no significant difference between the symptom-
atic group and asymptomatic group in age (p=0.63), gender
(p=0.17), BMI (p=0.20) and AAS (p=0.15).
UTC measurements
UTC analyses showed a distinct difference between the dis-
tribution of the four echo-types in the symptomatic group
versus the asymptomatic group. Figure 4 represents a typical
echo-type distribution of both groups in transversal view.
Quantitatively, the symptomatic group was significantly
different from the asymptomatic group for all echo-types
(table 1). Although there was some overlap between the
groups, symptomatic and asymptomatic tendons could be
clearly discriminated, for example, based on the percentage
of pixels in echo-types I+II (51.5% vs 76.6% in symptomatic
vs asymptomatic, p<0.001; table 1, fi g. 5). A difference in
mean tendon thickness between symptomatic and asymp-
tomatic tendons could also be observed (9.2 vs 6.8 mm in
symptomatic vs asymptomatic, p<0.001; table 1).
When a threshold of 75% in echo-types I+II is chosen (see
dotted line in fig. 5), three symptomatic tendons are above

Figure 4 Difference of an ultrasonographic tissue characterisation-processed image between an (A) asymptomatic tendon and (B) a
symptomatic tendon in transversal view. The border of the Achilles tendon, which was defined on the grey-scale image, is drawn with the white
line. Green pixels represent echo-types I, blue pixels echo-types II, red pixels echo-types III and black pixels echo-types IV. Note the frequently
observed increased echo-types III and IV on the posteromedial side within the asymptomatic tendon and the diffuse distribution within the
symptomatic tendon.

Table 1 Mean percentage of the separate four echo-types and tendon thickness are denoted for the
symptomatic and asymptomatic tendons
Symptomatic Asymptomatic
tendons (n=26) tendons (n=26)
Echo-types Mean SD Mean SD p Value ICC

%I 33.9 12.7 48.4 12.3 <0.001 0.92

% II 17.6 4.9 28.3 7.4 <0.001 0.92
% III 20.9 7.5 12.5 7.9 <0.001 0.95
% IV 27.5 11.1 10.8 7.6 <0.001 0.95
% I + % II 51.5 16.4 76.6 15.1 <0.001 0.95
% III + % IV 48.4 16.4 23.4 15.1 <0.001 0.95
Tendon anterior–posterior diameter (mm) 9.2 1.7 6.8 1.2 <0.001 0.84

Echo-types I+II (structure-related) and II+IV (non-structure-related) are grouped. The p values for the difference between
symptomatic and asymptomatic tendons and intraclass correlation coefficient (ICC) values for the two observers are also
presented for the echo-types and mean tendon thickness. The difference in all measured ultrasonographic tissue characteri-
sation parameters between symptomatic and asymptomatic tendons was statistically significant.

1156 Br J Sports Med 2010;44:1153–1159. doi:10.1136/bjsm.2009.061010


Figure 5 The distribution of the percentages of echo-types I+II in symptomatic and asymptomatic tendons. A clear discrimination can be made
between both groups. With a threshold of 75% echo-types I+II (dotted line), three tendons in the symptomatic group were above this threshold
and six tendons in the asymptomatic group were below this threshold (dark bars). The other 43 tendons (grey bars) had a tendon structure that
could be expected (abnormal structure in symptomatic tendons and normal structure in asymptomatic tendons).
this threshold and six asymptomatic tendons are under this
threshold (table 2). Thus, nine of the totally 52 tendons were
categorised in another group than expected, based on the UTC
fi ndings. With 43 tendons that were categorised as expected,
an accuracy of 83% was found.
The ICC values for the UTC parameters are presented in
table 1.
DISCUSSION
This is the fi rst study that quantifies tendon structure in
patients with Achilles tendinopathy and controls with use
of UTC. Symptomatic tendons showed significantly less sta-
bility of transverse echo patterns (less echo-types I+II) than
asymptomatic tendons (p<0.001). The mean AP tendon thick-
ness was 9.2 mm in the symptomatic group and 6.8 mm in
the asymptomatic group (p<0.001). The inter-observer reli-
ability of determining the UTC parameters was excellent (ICC
0.92–0.95) for quantification of the ultrasonographic tendon
structure. This indicates that different observers examining
the same tendon have excellent agreement between their fi nd-
ings; a prerequisite for implementation of UTC in the clinical
setting. For the evaluation of the tendon AP thickness, an ICC
of 0.84 was found.
Recently, other researchers focused on quantifying ten-
don integrity.13 14 For instance, Bashford et al13 attempted to
quantify structural changes in tendon tissue by analysing
the anisotropy of the speckle pattern of the ultrasonographic
image. Anisotropy of tendons is based on their unique archi-
tecture with tendon bundles organised in longitudinal align-
ment. As such, this approach is fairly similar to UTC since both
methods aim to isolate exclusively structure-related informa-
tion from a “speckle pattern”. As a consequence of anisot-
ropy, ultrasonography of tendons is sensitive for the tilt of the
transducer, possibly leading to a hypoechoic representation of
Br J Sports Med 2010;44:1153–1159. doi:10.1136/bjsm.2009.061010
Original article
Table 2 The number of tendons that were symptomatic and
asymptomatic are given
Normal tendon Abnormal tendon
structure structure
Asymptomatic tendon 20 6 26
Symptomatic tendon 3 23 26
23 39 52
With use of the threshold of 75% echo-types I+II, these tendons were divided
in groups with normal (>75% echo-types I+II) or abnormal (<75% echo-types
I+II) tendon structure. Three tendons in the symptomatic had a normal tendon
structure and six tendons in the asymptomatic group had an abnormal tendon
structure. The other 43 of totally 52 tendons were expected to be below the
threshold (symptomatic tendons) or above the threshold (asymptomatic tendons).
Therefore, ultrasonographic tissue characterisation has an accuracy of 83%
((43/52)×100%).
normal tendons. 24 25 In case of UTC, this artefact is prevented
by the tracking device with the transducer clamped in stan-
dardised position, in alignment and perpendicular to the ten-
dons long-axis and with fi xed transducer-tilt in the transverse
plane. The foot was supported with the ankle joint in a maxi-
mum dorsiflexion which prevented a sag of the Achilles ten-
don as much as possible and thus resulted in an optimal angle
of insonation. With this technique, only small tilting (lower
than 3°) may have occurred. From previous equine studies, it
is known that transducer tilting within 3° can result in small
variations in grey level. 26 However, with the use of UTC, the
outcome in echo-types is determined with the relative grey
value of the contiguous pixels and not the absolute grey value.
Therefore, small tilting would have no effects on the echo-
types measured with UTC.
In the study of Bashford et al,13 tendinopathic and healthy
tendons could be discriminated with an accuracy of 80%.
With optimal settings, an accuracy of 83% was found with
1157
 Original article
use of UTC in this study, which is comparable with the study
of Bashford et al13 (fig. 5 and table 2). The advantage of UTC is
that a connection with underlying tissue histology was made
with this approach in equine tendons.
The normal Achilles tendon has a more or less fl attened
ellipsoid shape with the axis through maximum AP thickness
frequently somewhat oblique, from antero-lateral towards
postero-medial. Therefore, we decided not to measure the
maximum AP thickness in the sagittal plane but rather in the
transverse image, thus independent of angle of insonation.
Maximum AP thickness was defi ned as the maximum
diameter perpendicular to the maximal latero-medial width
(fig. 3D). In the great majority of diseased tendons at least some
increase of cross-sectional area can be observed. Therefore, it
is relevant to measure the antero-posterior thickness. Aström
et al27 found that a thickness over 10 mm may be related to
the presence of a partial rupture. However, it should be noted
that these dimensions do not provide information about the
tendon structure. With the use of UTC, the dimension was
measured manually; and maybe, therefore, the inter-observer
reliability was not as excellent as measured by Syha et al, 28
who used an automatic identification procedure. With their
approach, an inter-reader variability of 3.9% was found.
UTC has clear advantages over conventional ultrasonog-
raphy, as UTC directly visualises and quantifies integrity.
Moreover, the grey levels in contiguous transverse echo pat-
terns are not an absolute value but rather a relative one, namely
their stability along the tendon long axis which is independent
of the ultrasonographic gain settings. This stability refers to
stability of the echo pattern in consecutive transverse sec-
tions and is thereby a true three- dimensional measure.
Furthermore, the tracking device prevented the transducer
from tilting; thus, the angle of insonation is standardised and
stable. The use of the tracking and data- collection system did
not only prevent a tilting artifact 24 25 but also facilitated the
storage and subsequent compounding of transverse images.
There are some limitations in this study. For instance,
the group of symptomatic tendons had already been unsuc-
cessfully treated with a heavy load eccentric exercise pro-
gram. Öhberg and Alfredson 29 reported in an observational
follow-up study that all 41 tendons of 30 patients had struc-
tural ultrasonographic changes (hypoechoic area or irregular
fibre structure). After follow-up (mean 28 months) with a
12-week eccentric exercise program, 37 of 41 tendons had
a normalised tendon structure. It is possible that this treat-
ment may alter the tendon structure and, therefore, result
in an improved echo pattern in some symptomatic tendons.
Similarly, we cannot exclude that a certain degree of degen-
eration could have been present in the asymptomatic group.
Subjects were included simply by asking if the subjects never
had complaints in the Achilles tendon region, while stricter
criteria could have been used. From post mortem studies, it
is known that asymptomatic tendon degeneration is pres-
ent in approximately 30%. 30 This may implicate that a cer-
tain degree of degeneration could have been present in the
asymptomatic group. Based on the anatomical similarities
between animal and human tendons, 31 the UTC echo-types
in human tendons can be expected to be similar to horse
tendons. Further analyses that relate UTC outcomes with
histology from human Achilles tendon material (eg, from
patients undergoing surgery) might corroborate tissue char-
acterisation by UTC. Reference sets for different age, gender
and activity level might be needed to precisely determine
the clinical relevance.
1158
The UTC procedure could be even more standardised
with standard dorsiflexion of the ankle joint and improved
tracking- and data-collection device. As such, UTC might
be a very useful quantitative method for the monitoring and
evaluation of existing and new treatment protocols for tendi-
nopathy. In addition, it would be very valuable to determine
its prognostic value.
CONCLUSION
UTC was transferred from equine-validated tests to human
Achilles tendons. The method showed excellent inter-
observer reliability and a significant difference in quantified
echo-types between symptomatic and asymptomatic ten-
dons, indicating its value for the evaluation of treatment in
tendinopathy.
Competing interests None.
Patient consent Obtained.
Ethics approval This study was conducted with the approval of the Medical Ethics
Committee METC Zuid-West Holland.
Provenance and peer review Not commissioned; externally peer reviewed.
What is already known on this topic
▶ An ultrasonographic observation in tendinopathic
tendons is the presence of a hypoechoic lesion. However,
ultrasonography is essentially based on a qualitative
assessment, and transducer handling and machine settings
do influence echogenicity and size of the hypoechoic lesion
to a large extent. Ultrasonographic tissue characterisation
(UTC) is a valuable technique to quantify the integrity of
tendon tissue in the horse, with histology as reference test.
What this study adds
▶ In this study, UTC was applied for the first time in
human Achilles tendons. There was an excellent inter-
observer reliability when evaluating the images and a
significant difference in quantified echo patterns between
symptomatic and asymptomatic Achilles tendons.
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